Evidence for the prepattern/cooption model of vertebrate jaw evolution
Language English Country United States Media print-electronic
Document type Journal Article, Research Support, N.I.H., Extramural, Research Support, Non-U.S. Gov't
Grant support
R01 DE017911
NIDCR NIH HHS - United States
DE017911
NIDCR NIH HHS - United States
PubMed
20855630
PubMed Central
PMC2951391
DOI
10.1073/pnas.1009304107
PII: 1009304107
Knihovny.cz E-resources
- MeSH
- Biological Evolution * MeSH
- Models, Biological * MeSH
- Jaw anatomy & histology MeSH
- Homeodomain Proteins genetics metabolism MeSH
- Lampreys * anatomy & histology genetics MeSH
- Molecular Sequence Data MeSH
- Vertebrates anatomy & histology genetics MeSH
- Body Patterning MeSH
- Basic Helix-Loop-Helix Transcription Factors genetics metabolism MeSH
- Transcription Factors genetics metabolism MeSH
- Gene Expression Regulation, Developmental MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, N.I.H., Extramural MeSH
- Names of Substances
- Distal-less homeobox proteins MeSH Browser
- Homeodomain Proteins MeSH
- Basic Helix-Loop-Helix Transcription Factors MeSH
- Transcription Factors MeSH
The appearance of jaws was a turning point in vertebrate evolution because it allowed primitive vertebrates to capture and process large, motile prey. The vertebrate jaw consists of separate dorsal and ventral skeletal elements connected by a joint. How this structure evolved from the unjointed gill bar of a jawless ancestor is an unresolved question in vertebrate evolution. To understand the developmental bases of this evolutionary transition, we examined the expression of 12 genes involved in vertebrate pharyngeal patterning in the modern jawless fish lamprey. We find nested expression of Dlx genes, as well as combinatorial expression of Msx, Hand and Gsc genes along the dorso-ventral (DV) axis of the lamprey pharynx, indicating gnathostome-type pharyngeal patterning evolved before the appearance of the jaw. In addition, we find that Bapx and Gdf5/6/7, key regulators of joint formation in gnathostomes, are not expressed in the lamprey first arch, whereas Barx, which is absent from the intermediate first arch in gnathostomes, marks this domain in lamprey. Taken together, these data support a new scenario for jaw evolution in which incorporation of Bapx and Gdf5/6/7 into a preexisting DV patterning program drove the evolution of the jaw by altering the identity of intermediate first-arch chondrocytes. We present this "Pre-pattern/Cooption" model as an alternative to current models linking the evolution of the jaw to the de novo appearance of sophisticated pharyngeal DV patterning.
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Gans C, Northcutt RG. Neural crest and the origin of vertebrates: A new head. Science. 1983;220:268–273. PubMed
Clouthier DE, Schilling TF. Understanding endothelin-1 function during craniofacial development in the mouse and zebrafish. Birth Defects Res C Embryo Today. 2004;72:190–199. PubMed
Walshe J, Mason I. Fgf signalling is required for formation of cartilage in the head. Dev Biol. 2003;264:522–536. PubMed
Thomas T, et al. A signaling cascade involving endothelin-1, dHAND and msx1 regulates development of neural-crest-derived branchial arch mesenchyme. Development. 1998;125:3005–3014. PubMed
Miller CT, Yelon D, Stainier DY, Kimmel CB. Two endothelin 1 effectors, hand2 and bapx1, pattern ventral pharyngeal cartilage and the jaw joint. Development. 2003;130:1353–1365. PubMed
Walker MB, Miller CT, Coffin Talbot J, Stock DW, Kimmel CB. Zebrafish furin mutants reveal intricacies in regulating Endothelin1 signaling in craniofacial patterning. Dev Biol. 2006;295:194–205. PubMed
Depew MJ, Lufkin T, Rubenstein JLR. Specification of jaw subdivisions by Dlx genes. Science. 2002;298:381–385. PubMed
Talbot JC, Johnson SL, Kimmel CB. hand2 and Dlx genes specify dorsal, intermediate and ventral domains within zebrafish pharyngeal arches. Development. 2010;137:2507–2517. PubMed PMC
Walker MB, Miller CT, Swartz ME, Eberhart JK, Kimmel CB. phospholipase C, beta 3 is required for Endothelin1 regulation of pharyngeal arch patterning in zebrafish. Dev Biol. 2007;304:194–207. PubMed PMC
Jeong J, et al. Dlx genes pattern mammalian jaw primordium by regulating both lower jaw-specific and upper jaw-specific genetic programs. Development. 2008;135:2905–2916. PubMed PMC
McCauley DW, Bronner-Fraser M. Neural crest contributions to the lamprey head. Development. 2003;130:2317–2327. PubMed
McCauley DW, Bronner-Fraser M. Importance of SoxE in neural crest development and the evolution of the pharynx. Nature. 2006;441:750–752. PubMed
Langille RM, Hall BK. Role of the neural crest in development of the trabeculae and branchial arches in embryonic sea lamprey, petromyzon marinus (L) Development. 1988;102:301–310.
Shu DG, et al. Head and backbone of the Early Cambrian vertebrate Haikouichthys. Nature. 2003;421:526–529. PubMed
Gess RW, Coates MI, Rubidge BS. A lamprey from the Devonian period of South Africa. Nature. 2006;443:981–984. PubMed
Meulemans D, Bronner-Fraser M. Amphioxus and lamprey AP-2 genes: Implications for neural crest evolution and migration patterns. Development. 2002;129:4953–4962. PubMed
Cerny R, et al. Developmental origins and evolution of jaws: New interpretation of “maxillary” and “mandibular”. Dev Biol. 2004;276:225–236. PubMed
Takio Y, et al. Hox gene expression patterns in Lethenteron japonicum embryos—insights into the evolution of the vertebrate Hox code. Dev Biol. 2007;308:606–620. PubMed
Shigetani Y, Sugahara F, Kuratani S. A new evolutionary scenario for the vertebrate jaw. Bioessays. 2005;27:331–338. PubMed
Neidert AH, Virupannavar V, Hooker GW, Langeland JA. Lamprey Dlx genes and early vertebrate evolution. Proc Natl Acad Sci USA. 2001;98:1665–1670. PubMed PMC
Myojin M, et al. Isolation of Dlx and Emx gene cognates in an agnathan species, Lampetra japonica, and their expression patterns during embryonic and larval development: Conserved and diversified regulatory patterns of homeobox genes in vertebrate head evolution. J Exp Zool. 2001;291:68–84. PubMed
Kuraku S, Takio Y, Sugahara F, Takechi M, Kuratani S. Evolution of oropharyngeal patterning mechanisms involving Dlx and endothelins in vertebrates. Dev Biol. 2010;341:315–323. PubMed
Sauka-Spengler T, Meulemans D, Jones M, Bronner-Fraser M. Ancient evolutionary origin of the neural crest gene regulatory network. Dev Cell. 2007;13:405–420. PubMed
Charité J, et al. Role of Dlx6 in regulation of an endothelin-1-dependent, dHAND branchial arch enhancer. Genes Dev. 2001;15:3039–3049. PubMed PMC
Robinson GW, Mahon KA. Differential and overlapping expression domains of Dlx-2 and Dlx-3 suggest distinct roles for Distal-less homeobox genes in craniofacial development. Mech Dev. 1994;48:199–215. PubMed
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn. 1995;203:253–310. PubMed
Kuraku S, Kuratani S. Time scale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences. Zoolog Sci. 2006;23:1053–1064. PubMed
Cohn MJ. Evolutionary biology: Lamprey Hox genes and the origin of jaws. Nature. 2002;416:386–387. PubMed
Kuraku S, Meyer A, Kuratani S. Timing of genome duplications relative to the origin of the vertebrates: Did cyclostomes diverge before or after? Mol Biol Evol. 2009;26:47–59. PubMed
Schaffer J. Uber das knorpelige skelett von Ammocoetes branchialis nebst Bemerkungen ueber das knorpelgewebe in Allgemeienen. Z Wiss Zool. 1896;61:606–615.
Wright GM, Youson JH. Ultrastructure of mucocartilage in the larval anadromous sea lamprey, Petromyzon marinus L. Am J Anat. 1982;165:39–51. PubMed
Gaskell WH. The Origin of Vertebrates. London: Longmans, Green, and Co.; 1908.
Martin WM, Bumm LA, McCauley DW. Development of the viscerocranial skeleton during embryogenesis of the sea lamprey, Petromyzon Marinus. Dev Dyn. 2009;238:3126–3138. PubMed
Morrison SL, Campbell CK, Wright GM. Chondrogenesis of the branchial skeleton in embryonic sea lamprey, Petromyzon marinus. Anat Rec. 2000;260:252–267. PubMed
Shigetani Y, et al. Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution. Science. 2002;296:1316–1319. PubMed
Takio Y, et al. Evolutionary biology: Lamprey Hox genes and the evolution of jaws. Nature. 2004;429:262. PubMed
Settle SH, et al. Multiple joint and skeletal patterning defects caused by single and double mutations in the mouse Gdf6 and Gdf5 genes. Dev Biol. 2003;254:116–130. PubMed
Tucker AS, Watson RP, Lettice LA, Yamada G, Hill RE. Bapx1 regulates patterning in the middle ear: Altered regulatory role in the transition from the proximal jaw during vertebrate evolution. Development. 2004;131:1235–1245. PubMed
Tribioli C, Lufkin T. The murine Bapx1 homeobox gene plays a critical role in embryonic development of the axial skeleton and spleen. Development. 1999;126:5699–5711. PubMed
Settle SH, Jr., et al. Multiple joint and skeletal patterning defects caused by single and double mutations in the mouse Gdf6 and Gdf5 genes. Dev Biol. 2003;254:116–130. PubMed
Storm EE, Kingsley DM. GDF5 coordinates bone and joint formation during digit development. Dev Biol. 1999;209:11–27. PubMed
Storm EE, Kingsley DM. Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development. 1996;122:3969–3979. PubMed
Stock DW, Whitt GS. Evidence from 18S ribosomal RNA sequences that lampreys and hagfishes form a natural group. Science. 1992;257:787–789. PubMed
Ota KG, Kuraku S, Kuratani S. Hagfish embryology with reference to the evolution of the neural crest. Nature. 2007;446:672–675. PubMed
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